Azizi et al. Malar J (2020) 19:114 https://doi.org/10.1186/s12936-020-03188-7 Malaria Journal

RESEARCH Open Access Malaria situation in a clear area of : an approach for the better understanding of the health service providers’ readiness and challenges for malaria elimination in clear areas Hosein Azizi1,2*, Elham Davtalab‑Esmaeili2, Mostafa Farahbakhsh2, Maryam Zeinolabedini3, Yagoub Mirzaei4 and Mohammad Mirzapour5

Abstract Background: Malaria mortality and morbidity have decreased in recent years. Malaria elimination (ME) and efective eforts to achieve ME is one of the most important priorities for health systems in countries in the elimination phase. In very low transmission areas, the ME programme is faced with serious challenges. This study aimed to assess the trend while getting a better understanding of Health Service Providers’ (HSPs) readiness and challenges for ME in a clear area of Iran. Methods: This study was performed in two phases. At frst, the malaria trend in , was sur‑ veyed from 2001 to 2018; afterward, it was compared with the national situation for a better understanding of the second phase of the study. Data were collected from the Ministry of Health’s protocol and the health centre of the province. In the second phase, malaria control programme experts, health system researchers, and health managers’ opinions were collected via in-depth interviews. They were asked regarding HSPs readiness and appropriate Malaria Case Management (MCM) in a clear area and possible challenges. Results: A total of 135 and 154,560 cases were reported in the last 18 years in East Azerbaijan Province and Iran, respectively. The incidence rate decreased in East Azerbaijan Province from 0.4/10,000 in 2001 to zero in 2018. Further‑ more, no indigenous transmission was reported for 14 years. Also, for the frst time, there was no indigenous transmis‑ sion in Iran in 2018. The main elicited themes of HSPs readiness through in-depth interviews were: appropriate MCM, holistic and role-playing studies for assessment of HSPs performance, system mobilization, improving identifcation and diagnosis of suspected cases in the frst line. Similarly, the main possible challenges were found to be decreas‑ ing health system sensitivity, malaria re-introduction, and withdrawing febrile suspected cases from the surveillance chain. Conclusion: Health systems in eliminating phase should be aware that the absence of malaria cases reported does not necessarily mean that malaria is eliminated; in order to obtain valid data and to determine whether it is

*Correspondence: [email protected] 1 Department of Epidemiology and Biostatistics, School of Health, Tehran University of Medical Sciences, Tehran, Iran Full list of author information is available at the end of the article

© The Author(s) 2020. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativeco​ ​ mmons.org/licen​ ses/by/4.0/​ . The Creative Commons Public Domain Dedication waiver (http://creativeco​ mmons​ .org/publi​ cdoma​ in/​ zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Azizi et al. Malar J (2020) 19:114 Page 2 of 10

eliminated, holistic and role-playing studies are required. Increasing system sensitivity and mobilization are deemed important to achieve ME. Keywords: Challenges, Elimination, Iran, Malaria, Readiness, Health service provider

Background understood. Tus, advances in understanding local According to the World Health Organization (WHO) and up-to-date information about malaria trends and report in 2018, malaria mortality and morbidity have situations in clear areas are essential for the National decreased in recent years [1]. In 2017, the number of Malaria Control Programme and health policymak- malaria deaths was reduced from 607,000 to 435,000 ers in countries in the elimination phase. Another aim compared to 2010, also, during these years the global of this study is to assist policymakers in better under- incidence rate of malaria reduced from 72 to 59 cases per standing of system readiness and challenges for ME 1000 population at risk [2]. Many countries in the world as well as adopting an appropriate strategy to adjust made substantial progress in malaria elimination (ME). barriers and challenges in clear areas [14]. Hence, the Te WHO has defned that ME is the interruption of present study aimed to investigate HSPs readiness and indigenous transmission of a specifed malaria parasite challenges for ME and malaria trends in East Azerbai- species in a defned geographic area; continued measures jan Province from 2001 to 2018. are required to prevent re-establishment of transmission [3, 4]. In Iran, during the last decades, malaria has been the Methods most important infectious disease with about 1500 cases Study design per year, especially, in southern and southeastern areas Tis study was performed in East Azerbaijan Prov- [5, 6]. ME was started with political commitment, inter- ince, northwest of Iran in which no Indigenous malaria sectional collaboration, and evidence-based research in case has been reported for 15 years (from 2005). Tis 2009 and Iranian health system is planning for ME certi- study was composed of two sections. In the frst sec- fcation in 2025 [7]. During the last decades, vector con- tion, malaria trend was investigated from 2001 to 2018 trol interventions as well as many efective eforts have in East Azerbaijan Province, an area of Iran considered been done for malaria control including enlarged cover- cleared of malaria. age of integrated vector management (IVM), using rapid In section two, 6 in-depth interviews were conducted diagnostic tests (RDTs), appropriate case management, with two malaria feld experts (one with master’s degree training of microscopists and Health Service Providers and the other a medical doctor), who monitored and (HSPs), and developing a malaria early warning system supervised malaria control programme, two were vice [7–9]. For the frst time, zero indigenous case reported managers and the other two were researchers with in Iran in 2018. A large amount of efective eforts, envi- PhD in health system from University of Medi- ronmental measures, and proper case management were cal Sciences. In Iran, medical universities are responsi- conducted for malaria control in Iran [10]. ble authorities for the health system in each province. In clear areas and countries in elimination phase, Te Iranian health system is composed of three levels system readiness, an appropriate malaria case manage- based on referral system; the frst level is primary level ment (MCM), such as identifcation, diagnosis, appro- of health services to access all urban and rural popula- priate treatment and urgent report of malaria cases to tions by family physicians and various types of HSPs. the public sector, and system vigilance were decreased When patients need special health services, they are [11]. In these areas, the management of suspected referred to the second level (county hospitals) by family malaria or febrile cases is defective due to the very low physicians, and when high special services are required, or absence of malaria transmission [12, 13]. Terefore, patients are referred to province referral hospitals with the sustainability of elimination status and appropriate high special services [15, 16]. It is worthwhile to men- MCM are necessary for pre-elimination. Based on the tion that in Iran all malaria control services in the pub- province malaria department data in northwest of Iran, lic sector such as diagnosis and treatment of malaria East Azerbaijan Province, the indigenous transmission cases are free and anti-malarial drugs are available only has been absent for 14 years and imported cases were in the public sector in the frst referral level. Te public very few. However, it seems that in clear areas, malaria sector is responsible for malaria control in Iran. Not to surveillance and HSPs readiness statuses are poorly mention that private sector has to report any identifca- tion of a suspected malaria case to public sector. Azizi et al. Malar J (2020) 19:114 Page 3 of 10

Defnitions the national situation for a better understanding of the Health service providers (HSPs) are primary health care Iranian malaria situation and malaria elimination pro- practitioners who visit people with common medical gramme goal with planning for elimination in 2025 and problems. HSPs are the frst line providers whom sus- receiving ME certifcation which is awarded for national pected malaria cases referred in the frst step. Tese geographical level. Fortunately, in most Iranian prov- providers comprised of emergency physicians, family inces, there is no indigenous malaria transmission. physicians, general practitioners, public or private sector Hence, the main objective of this study is to assess the specialists (in health centres, hospitals, and clinics), phar- HSPs readiness for ME in specifc regions (East Azerbai- macists, health workers, and health care providers in cit- jan Province) of Iran and to understand the challenges ies and villages. associated with ME in general. HSPs readiness in this study, readiness is relevant to HSPs practice and performance in the management In‑depth interviews of patients with a history compatible with suspected Te face to face in-depth interviews were conducted with malaria. HSPs readiness is a part of health system readi- 6 participants. Te interviews, lasting at least 1 h, were ness, and the aim of this study was an appropriate MCM audio-recorded and transcribed by two authors of the by HSPs including identifcation of suspected malaria present study; subsequently, the results were compared cases, correct diagnosis, prompt and appropriate treat- and scrutinized separately. Prior to using questions for ment according to the national guideline and urgent in-depth interviews, critical comments from three high report to the public sector. experts were obtained (a health worker, a researcher, and Role-playing method in the elimination phase, the an epidemiologist). Some questions were revised. Te malaria cases are rare or absent. Terefore, HSPs cannot interviews comprised two main parts including many demonstrate their actual performance for real malaria more in-depth questions. Te frst part was related to cases. Adjusting this barrier could be obtained through participants’ opinions regarding HSPs readiness for ME, using artifcial patients or standard cases in a role-play- HSPs performance in the case management of suspected ing design as a fake suspected malaria case. Accordingly, malaria, and the participants’ prediction and inference role-playing is the changing of one’s behaviour to assume about a real MCM status by HSPs in clear areas. Te sec- a suspected malaria case role to assess HSPs performance ond part focused on possible challenges encountered by in a realistic situation. provincial health services in the elimination phase. HSPs mobilization is a capacity-building process, Furthermore, the following detailed, as well as ad hoc encouragement and pro-activating HSPs in the case questions according to the interviewee’s answers and management of suspected malaria cases to improve the their level of expertise were asked under the frst part identifcation, early diagnosis, prompt and appropriate framework. (1) How much do you think that the prov- treatment, and control of malaria cases to quickly achieve ince’s health system is ready for ME? (2) How much HSPs the goal of elimination. are ready? (3) Do you think if a real febrile malaria patient Imported case malaria case or infection in which the were referred to providers, MCM would be done cor- infection was acquired outside the area in which it is rectly? (4) What are the main weaknesses in the appro- diagnosed. priate MCM? (5) Does the absence of local malaria cases Indigenous case A case contracted locally with no evi- provide evidence for local elimination? (6) What would dence of importation and no direct link to transmission be your recommendations to enhance system vigilance from an imported case. and HSPs Readiness? Under the framework of second part, following ques- tions were asked: (1) what do you think about ME chal- Data collection lenges in the province? (2) Which major challenge do you Malaria situation in East Azerbaijan, a clear area think is the most critical? (3) What eforts should be per- Te trend of malaria cases was obtained from the Min- formed for the stability of elimination status? (4) Do you istry of Health’s protocol and provincial malaria control think the health system is adequately alert and there is department and center for disease control. Provincial no concern for the re-introduction of malaria? (5) Is the Health Center is a deputy of health in Tabriz University health system and HSPs mobilized for ME? (6) Are there of Medical Sciences in East Azerbaijan and is responsi- enough literature and studies about ME available? ble for the malaria control programme among all urban and rural areas by many types of HSPs, laboratories and Analysis and interpretation of interviews environmental eforts. Malaria trend and malaria situ- After audio-recording and transcribing the interviews, ation in East Azerbaijan Province were compared with the audio-recorded fles were listened carefully and Azizi et al. Malar J (2020) 19:114 Page 4 of 10

transcripts were written in Persian by two authors. After- occurred in province and whole country were reported in wards, the main themes, topics, and terms were extracted 2001 and 2003, respectively. in each question and summarized in a brief explanation Among East Azerbaijan Province counties, Kaley- and interpretation by two experts. Interviews were read bar had the highest infection rate with 72 cases dur- and compared line by line and then divided into catego- ing the years of study (Table 2). Out of 135 malaria ries. Te core variable and main themes were extracted cases in the province, 86.67% and 51.11% were men and by the comparison between categories. In cases of mis- aged 31–40 years, respectively. Almost, 86% of malaria understanding, a member check was used. Te tran- patients in province lived in rural areas and 63% of them scripts were then translated into English by two experts were laborer. Furthermore, Plasmodium vivax was the while the names of interviewees were not indicated. dominant parasite species with 83.7% (Table 3). Table 4 demonstrates malaria screening (case fnding) trend by primary health care (PHC) in East Azerbaijan Results Province during 2004–2018. A total of 46,304 micro- Table 1 illustrates the malaria incidence between national scopic slides were taken and tested during the years of status and East Azerbaijan Province, a clear area of the study. Te fndings indicated that the numbers of sus- Iran, during 18 years from 2001 to 2018. Te number pected screened cases decreased whereas slide examina- of malaria cases decreased over the study period both tion (reading) in less than 48 h (the time interval between in-country and province, but the incidence rate in East preparation and microscopic examination increased Azerbaijan Province is lower than that in the rest of the from 2004 to 2018. country. Table 5 summarizes the main topic and themes of two A total of 135 and 154,560 cases were reported during interview parts respecting HSPs readiness and MCM in these years in East Azerbaijan Province and Iran, respec- a clear area as well as possible challenges in the elimi- tively. Te indigenous transmission was zero from 2005 nation phase. According to the recorded interviews and to 2018 in the province while in the whole country, it extracted results and interpretation, the following themes was zero for the frst time in 2018. Most malaria cases and categories were elicited.

Table 1 Trend of total malaria and Indigenous cases in Iran and East Azerbaijan province, 2001–2018 Years East Azerbaijan Iran Incidence rate­ b Total malaria Indigenous cases Incidence rate­ b Total malaria cases Indigenous cases cases

2001 0.4 40 19 3.1 19,129 a 2002 0.23 25 12 2.4 15,378 a 2003 0.3 35 29 3.8 25,027 a 2004 0.12 16 12 1.8 13,166 a 2005 0.04 6 0 2.8 19,285 14,634 2006 0.019 3 0 2.3 15,869 12,792 2007 0.018 2 0 2.3 16,489 12,538 2008 0.0063 1 0 1.6 11,333 6906 2009 0.02 4 0 0.8 5900 3606 2010 0 0 0 0.4 2965 1362 2011 0.0054 2 0 0.4 3108 1240 2012 0 0 0 0.2 1348 540 2013 0 0 0 0.2 1390 399 2014 0 0 0 0.16 1230 246 2015 0 0 0 0.1 777 156 2016 0 0 0 0.1 704 82 2017 0.0025 1 0 0.12 890 63 2018 0 0 0 0.07 572 0 Total 135 72 154,560 54,564 a Data not available b Per 10,000 persons at risk Azizi et al. Malar J (2020) 19:114 Page 5 of 10

Table 2 Distribution of malaria cases in counties of East Azerbaijan province, Iran, 2001–2018 County Years 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 2011 2012 2013 2014 2015 2016 2017 2018

Azarshahr 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 2 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 Ajabshir 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 Charoymaq 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 Jolfa 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 Sarab 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 Tabriz 0 0 0 0 0 0 1 1 0 0 0 0 0 0 0 0 0 0 19 12 29 12 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 2 1 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 1 2 1 2 0 1 0 0 0 0 1 0 0 0 0 0 0 0 Miyaneh 15 9 0 1 0 0 0 0 2 0 0 0 0 0 0 0 0 0 Hashtrud 1 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 Varzeqan 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 Total 40 25 35 16 6 3 2 1 4 0 2 0 0 0 0 0 1 0

Table 3 Demographic characters of malaria cases in East Azerbaijan, Iran, 2001–2018 Variables N 135 % = Table 4 Malaria screening (case fnding) trend in East Gender Azerbaijan province by primary health care, 2004–2018 Female 18 13.33 Years Numbers screening rate/1000 Slide examination Male 117 86.67 of slides­ a less than 48 h (%)b Age groups 2004 7412 5.5 33 20 8 5.92 ≤ 2005 5638 3.88 34.5 21–30 46 34.07 2006 4778 3.02 35.8 31–40 69 51.11 2007 3415 1.75 39.7 > 40 12 8.88 2008 2460 1.1 41.5 Residence 2009 2339 0.78 43.8 Urban 19 14.07 2010 1739 0.49 56.9 Rural 114 85.93 2011 1631 0.44 57.4 Occupation 2012 2013 0.53 73.8 Laborer 85 62.96 2013 2366 0.71 84 Housewife 18 13.33 2014 2604 0.68 87 Farming or farming related 9 6.66 2015 2427 0.63 90 Others 23 17.04 2016 3007 0.77 87 Parasite species 2017 2623 0.67 90.2 P. vivax 113 83.7 2018 1852 0.46 89 P. falciparum 20 14.81 Total 46,304 1.427 (mean) 62.90 (mean) P. malariae 0 0 a P. vivax P. falciparum 2 1.48 Slides were taken from febrile cases or subjects how had travel history to the + endemic areas b Slide examination is a period between slide preparation and lab investigation Azizi et al. Malar J (2020) 19:114 Page 6 of 10

Table 5 Extracted main topic and themes from in-depth interviews in relation to HSPs readiness and challenges for malaria elimination in a clear area of Iran Topics of in-depth interviews The main themes

Part 1) Health service providers readiness Inappropriate malaria case management Low holistic and role-playing studies about system readiness and health service providers performance in clear areas Quality of malaria identifcation and diagnosis Need to health worker re-training, system mobilization and support Part 2) Challenges of clear areas in elimination phase Decreasing of health system sensitivity due to absent of malaria cases Possibility of malaria re-introduction and neighbor countries with endemic situation Exiting febrile suspected cases from system surveillance chain

HSPs readiness and malaria case management System mobilization Appropriate malaria case management Most of the participating experts highlighted the need According to the participants’ views, if a real case of to a capacity-building process for system and HSPs malaria refers to HSPs, it may not be managed correctly. mobilization in clear areas. In order to access ME crite- Participants pointed out that there were many criteria ria, the following procedures should be put into sched- for correct MCM including eliciting travel history from ule: encouragement and mobilization of the health febrile cases, requesting appropriate diagnosis tests, system and HSPs, training and re-training programmes, providing appropriate treatment in less than 12 h and strengthening system support, and intersectional preparing urgent report to public health sector. Also, par- collaborations. ticipants expressed their concerns regarding febrile sus- pected MCM based on assessed knowledge and practice Malaria elimination challenges in clear areas of HSPs in the feld. Besides, the interviewees asserted System sensitivity that when febrile suspected malaria referred to HSPs, System sensitivity reduction was participants’ major con- most of the time, they were not assessed for malaria cern. Te reduced system sensitivity is described as the and there existed several shortcomings in the process of lower accuracy of the health system and HSPs in case of identifying patients with suspected malaria. As a result, identifcation of suspected malaria cases. Tis is due to sometimes, febrile cases were treated for endemic febrile very low malaria transmission in the elimination phase. diseases without being assessed for malaria morbidity in In recent years, malaria cases were absent and MCM the frst place. or readiness for ME was ignored, particularly, no local transmission has been reported in East Azerbaijan Prov- Holistic and role‑playing studies ince for 15 years. It seems that the health system and Interviewees believed that holistic, role playing, and KAP HSPs pay less attention to malaria recently. studies were required to evaluate HSPs performance, practice, attitude, and knowledge in the management of Possibility of re‑introduction febrile suspected malaria cases in clear areas. Due to the Interviewees’ other concerns and challenges pertained to absence of a real malaria patient in the elimination phase, the possibility of malaria re-introduction in one or two performing a study through using a role-playing tech- counties of the province (Kaleybar) as well as the neigh- nique could provide better understanding of the disease bourhood countries with endemic areas such as Pakistan control situation according to participants. and Afghanistan. Insecticide resistance, swamp areas and underdeveloped agricultural land in some places were Malaria identifcation and diagnosis raised as other concerns. In addition, interviewees commented on the quality of blood smears has been deteriorated over the last years. Exiting febrile suspected cases from system surveillance Sometimes, a thin and a thick spread of smears by frst chain line HSPs were not acceptable. Based on patient fow, One of the participants emphasized that in the current RDTs and anti-malarial drug availability should be health system condition, there existed many signifcant emphasized and considered important in sections with clinics in the private sector that could provide medi- higher possibility of suspected malaria cases such as cal care for malaria cases without appropriate MCM emergency departments, clinics, and public sectors. or sending any report. Needless to say that MCM is Azizi et al. Malar J (2020) 19:114 Page 7 of 10

acceptable only when it is done by the public sector and expanded coverage of integrated vector management zero reporting does not imply there is no malaria case. In (IVM), urgent report system, appropriate case manage- this regard, participants were in the opinion that efective ment, training of microscopists, developing a malaria coordination between private and public sectors were early warning system, rural malaria mobile teams, and required up until the time that, no suspected cases exited enhanced inter-sectoral collaborations are mentioned [7, from system surveillance. 9, 20]. After the ME programme’s national launch in 2009, this Discussion programme was strongly reinforced. Consequently, efec- Te present study investigated 18 years trend of malaria tive vector control interventions were implemented such cases and indigenous transmission in a clear area (East as distribution of free insecticide-treated nets (ITN), Azerbaijan Province), compared with whole country periodic indoor residual spraying (IRS), insecticide resist- status. Te fndings revealed that malaria incidence was ance monitoring, using various larvicides, sibling species, seriously reduced with no occurrence of indigenous molecular study, use of plants for larval control, using transmission from 2005 to 2018 (14 years), in other bed nets and long-lasting impregnated nets, using RDTs, words, province has been in the elimination phase for development of environmental and socio-economic sta- many years. In Iran, also, for the frst time in 2018, indig- tus, including water pipe network, better housing, health enous transmission was not reported and it is considered and welfare amenities [9, 21–23]. a great success for the national ME goal. Kyrgyzstan, Sri Lanka, and Paraguay are countries that In Iran, malaria pre-elimination programme started have recently obtained the WHO certifcate of malaria in 2009 with WHO’s technical support [8]. Tis pro- elimination while the UAE is the frst country to obtain gramme was aimed to interrupt Plasmodium falcipa- that in the Middle East, [2]. In India, by streamline pro- rum transmission by the end of 2015 and to achieve a gramme planning, management, and improvement malaria-free country in 2025. During the past decades, malaria surveillance system, approximately the same vector control and other interventions were devised and strategies as the Iranian health system were utilized to implemented with the political commitment for malaria achieve the goal of malaria elimination by 2027, [24]. In control and pre-elimination. Surprisingly, in the last Saudi Arabia, the malaria control programme initiated 2 years (2018 and 2019), the number of indigenous cases in 1948 and some major achievements were made in this at the national level has reached to zero [7]. In Iran, pas- respect. At the moment, this programme is focused on sive and active case fnding among suspected cases with imported cases, P. falciparum resistance to chloroquine, relevant symptoms and epidemiological history such as border malaria, and vector resistance to insecticides [25]. fever and travel history applied in the current malaria In China, the malaria elimination programme was surveillance system. Te case fnding in Iran focuses on launched in 2010 to achieve zero indigenous cases in the passive case detection. By defnition, if a positive case is country by 2015 and to eliminate by 2020. To achieve found, active case detection of the patient’s surroundings malaria elimination phase, specifc requirements such is performed by the community health workers (Behvarz as timely malaria case detection, timely surveillance, in Persian) or volunteers by taking blood smears (slides) response to all malaria cases, treatment, anti-mosquito and RDTs. Laboratory personnel continuously examined interventions, strengthening people’s awareness, and microscopic slides for malaria diagnosis. Standard oper- capacity building for malaria diagnosis were assigned ating procedures were performed for quality assurance of [26]. malaria diagnostic tests on all positive and 10% of neg- Despite these remarkable accomplishments, there are ative slides [17, 18]. Initiated in 2009 in Iran, RDTs are challenges to achieve the goal of elimination. However, in ordinarily used when microscopic detection is not avail- clear areas, the main concern is pertinent to system sen- able, in outlying areas (> 50 km from malaria diagnostic sitivity reduction and inappropriate MCM. While sev- centers), outbreaks and among migrants [18]. Using this eral research studies were conducted regarding malaria process by trained volunteers in rural areas can play a trends and situation in Iran and endemic areas [7, 14, critical role in early case fnding. Te polymerase chain 27] a few were carried out in clear areas and investigated reaction (PCR) is used when there is a discrepancy their challenges and readiness for ME compared with the between microscopic slides and RDTs’ tests results or trend of malaria at the national level [28]. Moreover, in when both are negative; nonetheless, the clinical and epi- this study, PHC surveillance system in malaria identifca- demiological symptoms are in favour of malaria [7, 19]. tion and management were assessed between 2004 and In the last decades, many efective eforts performed to 2018. control malaria and to get closer to elimination criteria Te fndings indicated that the screening rate (by in Iran. To name a few as the most important strategies, slides) from febrile suspected cases decreased in contrast Azizi et al. Malar J (2020) 19:114 Page 8 of 10

to slide reading in less than 48 h period (from the time expressed by the interviewees; whereas, the quality of slide was taken until the microscopic examination was slides seems low in the frst line of referral system. By adjusted). It is noteworthy that most of the slides were defnition, most of these slides were taken by the frst prepared and tested in this interval time in the last years. line HSPs in PHC and mostly in rural areas. As malaria As stated before, East Azerbaijan is a clear area of cases were rare in the elimination phase, thus, the qual- malaria which is in the elimination phase. All 7 malaria ity of slides was lower. It is true that malaria RDTs are cases in the last 10 years were imported cases. Efective utilized, however, according to participants’ opinions, in eforts, political commitment, and improvement in iden- places with higher febrile patient fow (e.g. Emergency tifying and treating suspected cases were emphasized wards) RTDs have to be emphasized and utilized more. and implemented by national and provincial malaria con- In this regard, intensifed monitoring and evaluation of trol programme. all components of the health system, sentinel surveil- It is very vital for policymakers and health systems to lance, fnancial support, evidence-based research, com- obtain up-to-date information at local level for better munity engagement, and intersectional collaboration are understanding of how to meet ME criteria and ascertain essential elements to be assigned [33]. In the same way, an appropriate strategy for adjusting barriers and chal- a study from a low transmission area recommended that lenges. In-depth interviews with heath managers, malaria a positive feedback mechanism should be considered for control programme experts and researchers elicited HSPs based on their quality of performance to health ser- many novel viewpoints that could be considered as key vices [3]. messages to fulfll ME criteria in clear areas and countries in elimination phase. Possible challenges of clear areas in elimination phase Although a few participants declared that there was no HSPs readiness concern and challenge in ME in the province, many of Te majority of participants were in the opinion that in them emphasized the possible existing challenges on the clear areas appropriate MCM status was unknown and way to achieve the elimination criterion required to be more attention was required. Tey added that the ideal improved by the health system. way to demonstrate HSPs readiness and performance, is One noteworthy fnding that emerged from the inter- to get beneft from role playing technique through chang- views was related to the notion of decreasing system ing one’s behaviour to pretend to be a suspected malaria sensitivity in East Azerbaijan Province and in other clear case. Hence, it can keep track of HSPs performance in areas which was considered as the most signifcant chal- a real way. HSPs ought to assess all febrile patients and lenge for ME. It might be because malaria cases were outpatients systematically in terms of malaria morbidity seriously reduced and HSPs and health facility attend- risk. Similarly, this issue was raised in other studies from ance for malaria and suspected cases were diminished. endemic countries and low transmission areas while Furthermore, many managers and policymakers focused few studies from clear areas are available [13, 28–30], on non-communicable diseases. However, very few stud- although there exist globally serious defects in correct ies were conducted and the relation between decreasing MCM [12, 31, 32]. To put it another way, it is urgently system sensitivity and malaria identifcation and case required that interventions for appropriate MCM, espe- management were poorly understood. Some pieces of cially, in the private sector be applied. evidence support this notion [34, 35]. As a matter of fact, in low transmission areas and elimi- Another point raised by participants was regarding nation phases as well as the investigated province, KAP the possibility of malaria re-introduction in the province studies, particularly, to assess HSPs performance and due to two reasons; frst, in some counties of the prov- practice in role-playing situation are very low and in this ince, population are prone to malaria morbidity where province, no study was conducted. Perhaps, this might be weather and geographical conditions facilitate transmis- due to the absence of malaria cases. Health policymak- sion of this vector-borne disease. Second, the existence of ers need to realize the efect of their eforts and many malaria-endemic countries in the region and the possibil- aspects of the national malaria elimination programme ity of entrance by cases afected by malaria from Pakistan situation as well as ME criteria. Terefore, the current and Afghanistan; however, fortunately, illegal travellers study could be considered as a key path for ME. However, from endemic countries to East Azerbaijan Province are in order to obtain accurate and realistic information on rare. the status and readiness of areas in the elimination phase, One of the participants believed that in very low trans- community-based studies are required. mission areas, it was probable that febrile cases were Appropriateness of the rate of identifcation of malaria withdrawn from the malaria surveillance system. Despite from febrile or suspected cases was another point HSPs readiness, it is acceptable for ME that suspected Azizi et al. Malar J (2020) 19:114 Page 9 of 10

cases or febrile returning travellers directly refer to the Availability of data and materials Part of the data in this manuscript were qualitative and derived from in-depth pharmacy and clinicians in the private sector and receive interviews. Another part was obtained from aggregated and prepared data anti-fever drugs or be treated for other common related but it is available from the corresponding author on a reasonable request. diseases in the region. Globally, although this issue is Ethics approval and consent to participate a major concern in order to achieve elimination, it is The data in the study were attained from aggregated data and interviews with underestimated in the elimination phase. Another strik- experts, therefore the ethical participatory consent was not required. ing issue is pertinent to establishing coherence between Consent for publication public and private sectors in managing the patients with Interviewees agreed on the publication of results reported in this manuscript. suspected malaria. No patient is willing to subject her- self/himself to the inconvenience of a crowded public Competing interests The authors declare that there is no competing interests. sector with failures in service providing and low quality of services. Tus, some patients seek their medical needs Author details 1 in the private sector. Department of Epidemiology and Biostatistics, School of Health, Tehran University of Medical Sciences, Tehran, Iran. 2 Research Center of Psychia‑ try and Behavioral Sciences, Tabriz University of Medical Sciences, Tabriz, Iran. 3 Basic Sciences Department, School of Allied Medical Sciences, Tabriz Conclusion University of Medical Sciences, Tabriz, Iran. 4 Province Heath Center for Disease Control, Department of Communicable Diseases, Tabriz University of Medical Te current study explored 18 years trend of malaria and Sciences, Tabriz, Iran. 5 Health Network Manager, Tabriz University of Medical its situation in East Azerbaijan Province which is in the Sciences, Tabriz, Iran. elimination phase. In the last decade in this province, 7 Received: 10 August 2019 Accepted: 11 March 2020 malaria cases were recorded which all were imported cases, however, this province enjoys much better condi- tions compared with national status. 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